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Helminth Parasites of the Balkan Green Lizard, Lacerta Trilineata Bedriaga 1886, from Bursa, Turkey

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Helminth Parasites of the Balkan Green Lizard, Lacerta Trilineata Bedriaga 1886, from Bursa, Turkey H. S. YILDIRIMHAN, C. R. BURSEY, F. N. ALTUNEL Turk J Zool 2011; 35(4): 519-535 © TÜBİTAK Research Article doi:10.3906/zoo-0910-1 Helminth parasites of the Balkan green lizard, Lacerta trilineata Bedriaga 1886, from Bursa, Turkey Hikmet Sami YILDIRIMHAN1,*, Charles Robert BURSEY2, Fayık Naci ALTUNEL1 1Uludağ University, Science and Literature Faculty, Department of Biology, 16059 Bursa - TURKEY 2Department of Biology, Pennsylvania State University, Shenango Campus, Sharon, Pennsylvania 16146, USA Received: 01.10.2009 Abstract: Th irty-eight Balkan green lizards, Lacerta trilineata, from Turkey were examined for helminths. Th ree species of Digenea, Plagiorchis elegans, Pleurogenoides medians, Brachylaemus sp. (metacercaria); 2 species of Cestoda, Oochoristica tuberculata and Mesocestoides sp. (tetrathyridium); and 6 species of Nematoda, Abbreviata abbreviata, Ascarops strongylina (larva in cysts), Falcaustra armenica, Oswaldocruzia fi liformis, Skrjabinelazia hoff manni, Skrjabinodon medinae, were found. Lacerta trilineata represents a new host record for each of the parasite species; Plagiorchis elegans, Brachylaemus sp., Oochoristica tuberculata, Mesocestoides sp., Abbreviata abbreviata, Ascarops strongylina (larva), Falcaustra armenica Skrjabinelazia hoff manni, and Skrjabinodon medinae are reported from Turkey for the fi rst time. Key words: Digenea, Cestoda, Nematoda, Balkan green lizard, Lacerta trilineata, Turkey Bursa (Türkiye) ilinden toplanan İri Yeşil Kertenkele (Lacerta trilineata, Bedriaga 1886)’nin helmint faunası Özet: 38 iri yeşil kertenkele Bursa’ dan (Türkiye) (Lacerta trilineata) helmintleri incelenmek üzere toplanmıştır. Bulunan türlerin 3’ü Digenea; Plagiorchis elegans, Pleurogenoides medians, Brachylaemus sp. (metacercaria), 2’si Cestoda; Oochoristica tuberculata, Mesocestoides sp. (tetrathyridium), 6’sı Nematoda; Abbreviata abbreviata, Ascarops strongylina (kist içinde larva), Falcaustra armenica, Oswaldocruzia fi liformis, Skrjabinelazia hoff manni, Skrjabinodon medinae grubuna aittir. Lacerta trilineata, her bir parazit türü için yeni konak kaydı olup, bu parazitler iri yeşil kertenkeleden ilk kez rapor edilmiştir. Plagiorchis elegans, Brachylaemus sp., Mesocestoides sp., Abbreviata abbreviata, Ascarops strongylina (larva), Falcaustra armenica, Skrjabinelazia hoff manni, Skrjabinodon medinae türleri Türkiye için yeni kayıttır. Anahtar sözcükler: Digenea, Cestoda, Nematoda, İri Yeşil Kertenkele, Lacerta trilineata, Bursa, Türkiye Introduction Caucasus, southwestern Iran, Syria, and Israel to elevations up to 650 m (Baran and Atatur, 1998). To Th e Balkan green lizard, Lacerta trilineata our knowledge, there are no reports of helminths in Bedriaga, 1886 (Lacertidae), is known from the L. trilineata. Th e purpose of this paper is to provide Adriatic Sea coast to the Balkan countries, Turkey, an initial helminth list for L. trilineata. * E-mail: [email protected] 519 Helminth parasites of the Balkan green lizard, İ Bedriaga 1886, from Bursa, Turkey Materials and methods 1927; Plagiorchis brauni Massino 1927; Plagorochis Th irty-eight specimens of Lacerta trilineata (23 loossi Massino 1927; Plagiorchis massino Petrov males, 15 females, mean snout-vent length = 42 and Tichonoff , 1927; Plagiorchis multiglandularis ± 4 mm, range 35-48 mm) were collected by hand Semenow, 1927; Plagiorchis skrajabini Massino 1927; 1996-1998 at Osmangazi (40°10ʹN, 29°01ʹE, 650 m Plagiorchis uhlworni Massino, 1927; Plagiorchis elevation), Bursa province, Turkey. Lizards were killed potanini Skrjabin, 1928; Plagiorchis eutamiatis Schulz, with an overdose of sodium pentobarbital. Th e body 1932; Plagiorchis casarci Mehra, 1937; Plagiorchis cavity was opened, and the digestive tract removed. ferrigunum Mehra, 1937; Plagiorchis eutamiatis Th e esophagus, stomach, small and large intestine, Zibethicus Vassiliev 1939; Plagiorchis extremus Strom, and lungs were opened and separately examined 1940; Plagiorchis strictus Strom, 1940; Plagiorchis for helminths under a dissecting microscope. fuji Ogata, 1941; Plagiorchis ptschelkini Sobolev, Nematodes were killed in hot saline solution, fi xed 1946; Plagiorchis petrovi Fediushin, 1949; Plagiorchis in 70% ethanol, and mounted in glycerol. Digeneans oscineus Sudarikov, 1950; Plagiorchis castoris Orloff and cestodes were fi xed in 70% ethanol, stained with et Moskalev, 1953; Plagiorchis blatnensis Chalupsky, iron-carmine as described by Georgiev et al. (1986), 1954; Plagirochis raabei Furmaga, 1956; Plagirochis cleared in clove oil, and mounted in Entellan®. stefanski Furmaga, 1956, Plagiorchis muris sensu Helminth identifi cation was based on keys given Prokopic and Genov, 1974; Plagiorchis proximus by Schmidt (1986) and Yamaguti (1961). Helminth sensu Prokopic and Genov, 1974; Plagiorchis cuculi voucher specimens were deposited in the helminth Schaldybin, Anikin, Budkin et Suslova, 1977) collection of Uludağ University Museum of Zoology, Prevalence and mean intensity: 1/38 (3%), 1 Bursa, Turkey. Lizard specimens were deposited in individual. the Department of Biology, Uludağ University, Bursa, Temporal distribution: 10 Jun 1996, 1 host with 1. Turkey. Site of infection: Small intestine. Lacerta trilineata Type host and type locality: House sparrow, Passer Bedriaga, 1886 domesticus, Germany (Rudolphi, 1802). Th irty-eight L. trilineata (23 males, 15 females), Additional Turkish records: None. Osmangazi, Turkey (6 collected in June 1996, 3 in May 1997, 1 in August 1997, 3 in May 1998, 7 in June Other reported hosts: Amphibia: yellowbelly 1998, 16 in July 1998, and 2 in October 1998). toad, Bombina variegata, (Prokopic and Krivanec, 1975); pool frog, Pelophylas lessonae, (reported as Rana esculenta, Prokopic and Krivanec, 1975); Results common frog, Rana temporaria, (Capuse, 1971); Plagiorchis elegans Reptilia: sand lizard, Lacerta agilis, (Shevechenko and Barabashova, 1958; Moravec, 1963; Capuse, (Rudolphi, 1802) Braun, 1902 1971; Lewin, 1992a; Shimalov et al., 2000; Sharpilo (Syn. Fasciola elegans Rudolphi, 1802; Fasciola et al., 2001; Borkovcova and Kopriva, 2004); cirratus Rudolphi, 1802; Distoma colubri natricis European green lizard, Lacerta viridis, (Capuse, intestinale Rudolphi, 1809; Distoma elegans 1971); viviparous lizard, Zootoca vivipara, (reported (Rudolphi, 1802) Rudolphi,1809; Distoma colubri as Lacerta vivipara, Lewin, 1992b; Shimalov et al., tesssellati Rudolphi, 1819; Distoma lacertae Rudolphi, 2000); European grass snake, Natrix natrix (Capuse, 1819; Distomum (Brachylaimus) elegans (Rudolphi, 1971); Aves: northern goshawk, Accipiter gentilis, 1802) Dujardin 1845; Distomum erraticum Linstow (Sitko, 1998); Eurasian sparrowhawk, Accipiter nisus, 1894; Plagiorchis cirratus (Rudolphi, 1802) Lühe, (Sitko, 1998); spotted sandpiper, Actitis macularius, 1899; Plagiorchis mentulatus (Rudolphi 1819) (Didyk et al., 2007); Balkal tean, Anas formosa, Stossich, 1904; Plagiorchis asperus Stossich, 1904; (Bykhovskaya-Pavlovskaya, 1962); mallard, Anas Plagiorchis notabilis Nicoll, 1909; Plagiorchis marii platyrhynchos, (Styczynska-Jurewicz, 1962); little Skrajabin, 1920; Plagiorchis blumbergi Massino stint, Calidris minuta, (Bykhovskaya-Pavlovskaya, 520 H. S. YILDIRIMHAN, C. R. BURSEY, F. N. ALTUNEL 1962); twite, Carduelis fl avirostris, (Massino, 1929); Jurewicz, 1962); Eurasian curlew, Numenius arquata, ruddy shelduck, Casarca ferruginea, (Mehra, 1937); (Bykhovskaya-Pavlovskaya, 1962); slender-billed black tern, Chlidonias nigra, (Massino, 1929); western curlew, Numenius tenuirostris, (Bykhovskaya- marsh harrier, Circus aeruginosus, (Bykhovskaya- Pavlovskaya, 1962); tuft ed duck, Nyroca fuligula, Pavlovskaya, 1953; Krasnolobova, 1987); northern (Styczynska-Jurewicz, 1962); Eurasian golden harrier, Circus cyaneus, (Krasnolobova, 1987); oriole, Oriolus oriolus, (Bykhovskaya-Pavlovskaya, pallid harrier, Circus macrourus, (Bykhovskaya- 1962); Eurasia scops owl, Otus scops, (Braun, 1902); Pavlovskaya, 1953; Krasnolobova, 1987); common osprey, Pandion haliaetus, (Krasnolobova, 1987); quail, Coturnix coturnix, (Bykhovskaya-Pavlovskaya , bearded reeding, Panurus biarmicus (Bykhovskaya- 1953); common raven, Corvus corax, (Massino, 1927); Pavlovskaya, 1962); great tit, Parus major, carrion crow, Corvus corone, (Mühling, 1896); rook, (Braun, 1902; Bykhovskaya-Pavlovskaya, 1962); Corvus frugilegus, (Braun, 1902); Eurasian jackdaw, house sparrow, Passer domesticus, (Braun, 1902); Corvus monedula, (Massino, 1927); corncrake, Eurasian sparrow, Passer montanus, (Bykhovskaya- Crex crex, (Macko, 1969); common cuckoo, Pavlovskaya, 1962); coal tit, Periparus ater, (Massino, Cucullus canorus, (Dubinia and Kulakova, 1960); 1929); honey buzzard, Pernis apivorus, (Ferrer et al., common house-martin, Delichon urbica, (Odening, 2004); ruff , Philomachus pugnax, (Bykhovskaya- 1961); great spotted woodpecker, Dendrocopos Pavlovskaya, 1962); black-billed magpie, Pica major, (Styczynska-Jurewicz, 1962); merlin, Falco pica, (Braun, 1902); glossy ibis, Plegadis falcinellus, columbarius, (Massino, 1927; Krasnolobova, 1987); (Bykhovskaya-Pavlovskaya, 1962); dunnock, peregrine falcon, Falco peregrinus, (Krasnolobova, Prunella modularis, (Styczynska-Jurewicz, 1962); 1987); Eurasian hobby, Falco subbuteo, (Bykhovskaya- Eurasian nuthatch, Sitta europaea, (Styczynska- Pavlovskaya, 1953; Styczynska-Jurewicz, 1962; Jurewicz, 1962); common tern, Sterna hirundo, Krasnolobova, 1987; Ferrer et al., 2004); Eurasian (Bykhovskaya-Pavlovskaya, 1962); common starling, kestrel, Falco tinnunculus, (Sitko, 1998); red-footed Sturnus
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